Download Conservation of Deep Pelagic Biodiversity

Review
Conservation of Deep Pelagic Biodiversity
BRUCE H. ROBISON
Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039-9644, U.S.A., email [email protected]
Abstract: The deep ocean is home to the largest ecosystems on our planet. This vast realm contains what
may be the greatest number of animal species, the greatest biomass, and the greatest number of individual
organisms in the living world. Humans have explored the deep ocean for about 150 years, and most of
what is known is based on studies of the deep seafloor. In contrast, the water column above the deep seabed
comprises more than 90% of the living space, yet less than 1% of this biome has been explored. The deep
pelagic biota is the largest and least-known major faunal group on Earth despite its obvious importance at
the global scale. Pelagic species represent an incomparable reservoir of biodiversity. Although we have yet
to discover and describe the majority of these species, the threats to their continued existence are numerous
and growing. Conserving deep pelagic biodiversity is a problem of global proportions that has never been
addressed comprehensively. The potential effects of these threats include the extensive restructuring of entire
ecosystems, changes in the geographical ranges of many species, large-scale elimination of taxa, and a decline
in biodiversity at all scales. This review provides an initial framework of threat assessment for confronting the
challenge of conserving deep pelagic biodiversity; and it outlines the need for baseline surveys and protected
areas as preliminary policy goals.
Keywords: biodiversity, conservation, deep-sea animals, pelagic habitat
Conservación de la Biodiversidad Pelágica Profunda
Resumen: El mar profundo es uno de los ecositemas más extensos en nuestro planeta. Este vasto dominio
contiene lo que pudiera ser el mayor número de especies animales, la mayor biomasa y el mayor número de
organismos individuales en el mundo viviente. Los humanos hemos explorado el mar profundo durante casi
150 años, y la mayor parte de lo que se conoce se basa en estudios del lecho marino profundo. En contraste,
la columna de agua encima del lecho comprende más de 90% del espacio para vivir, sin embargo se ha
explorado menos de 1% de este bioma. La biota pelágica profunda es el grupo faúnico más grande y el menos
conocido no obstante su importancia obvia a escala global. Las especies pelágicas representan un reservorio
incomparable de biodiversidad. Aunque aun falta que se descubra y describa a la mayorı́a de estas especies,
las amenazas a su existencia son númerosas y están incrementando. La conservación de la biodiversidad
profunda es un problema de proporciones globales que nunca ha sido abordado integralmente. Los efectos
potenciales de estas amenazas incluyen la reestructuración extensiva de ecosistemas enteros, cambios en la
distribución geográfica de muchas especies, eliminación de taxa y una declinación de la biodiversidad en
todas las escalas. Esta revisión proporciona un marco de referencia inicial de la evaluación de las amenazas
para confrontar el reti de conservar la biodiversidad pelágica profunda; y delı́nea la necesidad de muestreos
básicos y del establecimiento de áreas protegidas como metas preliminares.
Palabras Clave: animales de aguas profundas, biodiversidad, conservación, hábitat pelágico
Introduction
Deep-sea biologists usually acknowledge the voyage of
HMS Challenger (1872–1876) as the genesis of their dis-
cipline. Beforehand, debate boiled around whether or not
life had penetrated to ocean depths beyond a few hundred meters. Most scientists of the day believed that the
lack of light, the cold, and the great pressures of depth
Paper submitted April 14, 2008; revised manuscript accepted January 12, 2009.
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C 2009 Society for Conservation Biology
DOI: 10.1111/j.1523-1739.2009.01219.x
848
precluded the possibility of life in the deep. The Challenger expedition firmly established that abundant life
exists on the deep seafloor, and most of what is known
today about deep-sea biology stems from these benthic
discoveries. Less clear was the picture of life in the water column above the deep seabed. For many additional
decades, most naturalists believed that pelagic animals
were restricted to two narrow zones—near the surface
and near the bottom. What has been learned in the last
60 years has begun to fill in the gap, and it is now clear
that the oceanic water column is filled with life.
The largest living space on Earth lies between the
ocean’s sunlit upper layers and the dark floor of the deep
sea, on average some 4000 m below the surface (Fig. 1).
Within this vast midwater habitat are the planet’s largest
animal communities, composed of creatures adapted to a
fluid, three-dimensional world without solid boundaries.
These animals probably outnumber all others on Earth,
but they are so little known that their biodiversity has yet
to be even estimated. This is a huge planetary resource,
yet far less is known about these species than about the
constituents of any other major habitat.
Photosynthesis in the near-surface layers is the primary
source of nutrients that flow through the oceanic food
chain. Organic matter created in sunlight is transferred
downward through a complex, interwoven ecological
web, and ultimately to the deep seafloor. Phytoplankton
and other organic particles at the base of the web are
grazed by small crustaceans and gelatinous filter feeders.
These grazers are consumed by micronektonic fishes and
squids (Fig. 2) and by four types of abundant gelatinous
predators: medusae, siphonophores, ctenophores, and
chaetognaths. The next trophic step in the midwater food
web is another set of predators, including anglerfishes,
dragonfishes, squids, and another suite of gelatinous carnivores (Fig. 3). Although top predators like pinnipeds,
whales, tunas, and swordfish feed in midwater as deep as
1000 m or more, the deeper one goes the less is known
about midwater ecology and the animals that live there.
To avoid being eaten by visually cued predators near
the surface, many midwater animals undertake daily vertical migrations (Childress 1995; Robison 2003). Each
morning as the sun rises, they swim downward into the
protective darkness of deep water. In the evening they
move back into the upper layers, where they graze on
organic matter produced there, or feed on grazers. Given
the countless individuals involved in these movements,
they must be the largest animal migrations on Earth. Animals that live below 1000 m also rely on organic matter
generated near the surface, but the vertical distances are
too great for efficient migration, so they depend on food
that sinks or swims down to their level. Many deep-living
pelagic species undertake an ontogenetic vertical migration in their life cycle. Buoyant eggs or larvae rise to
the surface layers, where they undergo the first stages of
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Conserving Deep Pelagic Biodiversity
Figure 1. Graphic representation of ocean volume
relative to bottom depth. The curve shows the global
volume of water above seafloor depths ranging from
0 to 10.9 km (the Mariana Trench). The edge of the
continental shelf at roughly 200 m is the traditional
boundary of the deep sea, and animals out beyond
this margin are said to live in deep water. Ecological
depth zones of the oceanic water column: epipelagic,
upper 150–200 m; mesopelagic, down to 1000 m;
bathypelagic, 1–4 km; abyssopelagic, 4–8 km; hadal,
below 8 km. The displayed volumes of terrestrial and
benthic environments include the surface areas of the
dry land and the seafloor and the air or water above
to a height of 1 km. (Data source: UN 2008).
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Figure 2. Firm-bodied deep
pelagic animals: (a) gulper eel
(Saccopharynx); (b) fangtooth
(Anoplogaster); (c) viperfish
(Chauliodus); (d) anglerfish
(Caulophryne); (e) snipe eel
(Nemichthys); (f) blackdragon
(Idiacanthus); (g) mysid shrimp
(Gnathophausia); (h) octosquid
(Octopoteuthis).
development; as juveniles, they descend back down to
the adult depth range.
Because their prey reside in darkness, predatory midwater fish and squid frequently have highly developed
eyes—functional in even the dimmest illumination. Thus,
visual trickery is a common practice (Bush & Robison
2007). Many species are camouflaged or cryptically colored, others achieve near invisibility by being transparent, and some use mimicry to fool predators (Robison
1999). Below about 1000 m, the last photons of sunlight
disappear and the midwater animals that live very deep
are often blind or have primitive eyes that may detect
light but do not form images.
In the absence of sunlight, a great many deep pelagic
animals produce their own light through the chemical
process of bioluminescence. Midwater animals use this
light in a variety of ways. Anglerfishes and dragonfishes
employ luminous lures to attract prey. Lanternfishes and
hatchetfishes have ventral light-producing organs that
erase their silhouettes when predators try to spot them
from below. Other animals use distinctive light patterns
for recognition and finding mates. Many species use light
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Conserving Deep Pelagic Biodiversity
Figure 3. Gelatinous deep pelagic
animals: (a) benthopelagic
medusa (Benthocodon); (b)
holopelagic medusa (Solmissus);
(c) halyard siphonophore
(Apolemia); (d) undescribed
siphonophore; (e) undescribed
cydippid ctenophore; (f)
ctenophore (Beröe); (g)
larvacean (Bathochordaeus); (h)
transparent squid
(Helicocranchia).
to blind or confuse their attackers or to make them vulnerable to their own predators (Robison 1992). Bioluminescence is so widespread that it must be the most
common form of communication in the ocean (Widder
2002).
As depth increases the growing weight of the water
above creates enormous pressure, which is the primary
barrier to scientific operations in the deep sea. Although
the animals that live in deep water are well adapted to
high pressure and low temperatures, we humans must
protect ourselves and our instruments in order to investigate this harsh environment. The deep pelagic habitat
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has been a stable, relatively homogeneous environment
for millions of years, and its stability has led to a relatively narrow range of physiological tolerances among
the species adapted to live there.
One of the most significant discoveries of recent years
has been that gelatinous animals comprise a major portion of the deep pelagic fauna (Fig. 3). Prior to the introduction of deep-diving midwater vehicles, these animals were seriously underestimated by conventional sampling methods because nets destroy their fragile bodies
(Madin & Harbison 1978). We now know that jellies
are the dominant life forms within some broad depth
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zones. Technological advances in vehicles, instruments,
and imaging systems are rapidly improving our understanding of deep pelagic biology (Robison 2004).
The Importance of Deep Pelagic Animals
Deep pelagic animals comprise critical structural and
functional links in oceanic ecosystems. They are a principal food source for most commercially captured pelagic
species. Although the majority of midwater species have
not yet been described or their ecologies fully characterized, it is clear that the biodiversity of this global
fauna plays an essential role in maintaining ecosystem
integrity. The deep pelagic fauna comprises what may be
the largest reservoir of animal diversity on Earth. Diversity
promotes stability (Ives & Carpenter 2007), so protecting
the stability of an ecosystem that provides a major portion of the world’s food is obviously in our best interests.
Deep pelagic animals provide another vital ecosystem
service by serving as a huge carbon sink. They capture
carbon removed from the atmosphere by phytoplankton,
and they keep it at depth.
In addition to their ecological significance, these animals and their genetic libraries offer a global resource of
molecular solutions to nature’s challenges. They embody
the results of countless lines of evolutionary progress
over hundreds of millions of years. Marine species have
already been the source of many unique chemical compounds with the potential for commercial development
as pharmaceuticals, nutritional supplements, industrial
enzymes, and for use in biotechnology and agricultural applications. In particular, soft-bodied invertebrates
that lack robust physical defenses have provided bioactive compounds based on their chemical defenses (e.g.,
Munro et al. 1999; Pomponi 2001). The newly discovered
diversity of deep-living gelatinous species presents rich
potential for antibiotics, antiparasitics, anticancer agents,
and other pharmaceutical compounds.
The Conservation Issue
Despite its obvious importance, the ocean’s deep interior remains an unexplored frontier, more than a billion
cubic kilometers of living space “that we have barely
looked at and do not understand” (Kunzig 2003). A million or more undescribed species, with biological adaptations and ecological mechanisms not yet imagined, may
live within the vast volume of the deep-sea water column (Robison 2004). Although the deep sea has begun
to receive the attention of conservationists, their efforts
to date have focused chiefly on the deep seafloor and on
pelagic animals that live near the surface (Norse 2005a,
2005b; Ardron et al. 2008; Halpern et al. 2008). Conservation organizations and the research community have
worked successfully to protect deep-sea corals, and they
are working to further restrict destructive, deep bottom
trawling (Gianni 2004).
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This greatest unapprised reservoir of animal biodiversity in the ocean, however, has yet to be included in
the protective considerations of any conservation, research, or governmental organization. The principal concern here should be the prospect of undetected mass
extinctions, which threaten losses in ecosystem function, economic opportunity, and vital ecosystem services
(Ehrlich & Wilson 1991; Worm et al. 2006). Conservation
of biodiversity is gaining momentum as a global concern,
yet the greatest part of the biggest ecosystems on Earth
lacks representation in the conservation effort. It is time
to address this issue.
Threats
The diversity of deep pelagic animals is threatened by a
broad array of influences and circumstances. What follows is a characterization of these threats, surely incomplete, but necessary because to date this issue has been
virtually ignored. Some threats are general, others are
specific, and the particular ways that these factors might
influence the deep pelagic fauna and the types of animals that might be particularly susceptible have yet to
be investigated. Although the threats are presented here
individually, their effects can be cumulative and multiple threats can be interactive (Zeidberg & Robison 2007;
Halpern et al. 2008).
Climate Change
The warming of the ocean’s upper layers is producing direct and indirect effects on specific biotic groups
throughout the oceanic water column. Of particular concern is the alteration of historical patterns of primary
production in the ocean’s upper layers, the basic food
supply of the animals living below. As the upper layers
become warmer, the water column becomes more stratified, which inhibits the vertical mixing needed to replenish basic nutrients required for photosynthesis. On a
global scale, it appears that both phytoplankton biomass
and growth rates decline as the surface layers get warmer
(Behrenfeld et al. 2006). In addition to overall reduction
of organic material supplied to the oceanic food web,
climate models suggest that continued warming may also
result in a geographical shift of production from lower to
higher latitudes (Boyd & Doney 2002; Behrenfeld et al.
2006).
Rising temperatures have been implicated in shifting
the geographic distribution patterns of plankton and
fishes (Batten & Welch 2004; Perry et al. 2005), in the disruption of plankton communities (Richardson & Schoeman 2004; Hays et al. 2005), and in large-scale changes in
pelagic biodiversity (Beaugrand et al. 2002). They have
also been linked to invasive range expansions by top
predators (Zeidberg & Robison 2007). The ocean’s upper
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layers, because of their high productivity, are where the
larvae and juveniles of many deep-living species develop,
before returning to the adult depth range. Because these
early life-history stages may have narrow physiological
tolerances, rising surface temperatures may play a role
in altering the abundance and geographical distribution
of species that live far below the surface as adults. Likewise, the reproductive cycles of consumer species may
be tightly coupled to seasonal pulses of plankton production at the surface. Climate change has begun to disrupt
these linkages (Edwards & Richardson 2004), with negative effects at higher trophic levels.
Although most of these effects of climate change
have been measured only in coastal waters or in the
open ocean’s upper layers, it is likely that corresponding changes are occurring in the deeper parts of the
food web. In deep water we can also expect that climate
change will have large-scale effects by slowing down the
ocean’s major circulation patterns, reducing the oxygen
content at depth, and warming even the deepest layers.
The deep pelagic fauna has evolved within a stable physical environment and as a result they may be particularly
sensitive to such changes (Koslow 2007).
Carbon Dioxide
The oceans have a great chemical affinity for carbon dioxide, which is readily absorbed from the atmosphere. One
result of this affinity is the creation of carbonic acid and a
change in the balance of hydrogen ions, so that seawater
becomes more acidic when more CO 2 is absorbed. As atmospheric concentrations of CO 2 rise, one can expect to
see both direct and indirect effects of ocean acidification
on the deep pelagic biota. Increasing acidity will reduce
the availability of carbonate ions that are important to
coccolithophores and foraminifera at the base of pelagic
food webs and to crustaceans, some mollusks, and other
organisms with calcified shells or hard structures (Royal
Society 2005; Guinotte & Fabry 2008). Increasing CO 2
concentration in seawater can also lead to the same acidic
condition in body tissues and fluids (hypercapnia). Internal acidification affects the ability of blood to carry
oxygen and imposes other physiological stresses, including negative impacts on reproductive processes (Royal
Society 2005).
Direct injection of anthropogenic CO 2 into the ocean
has been proposed as a means of reducing its rate of accumulation in the atmosphere (Marchetti 1977). Whether it
is released as liquid to form a hydrate-covered lake on the
deep seafloor or is dispersed into the water column, CO 2
sequestered in this manner will likely have a profound impact on the deep-sea fauna. Here again, the principal effect will be to lower the pH of seawater and consequently
of the animals that live in it. Seibel and Walsh (2001) have
examined the potential effects of direct CO 2 injection on
the deep-sea biota, and they conclude that these animals
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are highly susceptible to the excursions of CO 2 and pH
that would accompany sequestration. Among the effects
are reduced oxygen uptake capacities. For example, under conditions where its arterial pH drops by just 0.2, the
deep-living pelagic shrimp Gnathophausia ingens (Fig.
2g) would experience a 50% reduction in the bound oxygen level in its blood (Childress & Seibel 1998). Additional
effects include metabolic suppression, a reduction in basic processes such as the protein syntheses necessary for
reproduction and growth.
Commercial Fishing
Removing top predators from the oceanic food chain has
already had a significant impact on pelagic ecosystems
(Frank et al. 2005; Worm et al. 2005, 2006). Although
high-seas fisheries are destined to continue because of
the growing world demand for protein, the ecological
consequences for untargeted, deep-living species have
almost never been considered, much less investigated.
Trophic cascades that restructure the food web at lower
trophic levels appear to be inevitable (Caddy & Rodhouse
1998; Myers et al. 2007). At the present time, the resulting changes to deep pelagic biodiversity are not measurable because too little is known about the trophic webs
and because there is insufficient baseline data to reveal
changes.
In the open ocean, many top predators feed on species
that migrate from deep water to the surface each night,
then down again during the day. Thus, the commercial
catch of top predators can directly impact deep-living
species through the removal of top-down controls. Nevertheless, predicting the effects on the deep-water community is presently beyond our understanding. If a harvested species is pushed to commercial or population
extinction, it may not recover when fishing stops. In
some cases an affected species may be replaced by others that fill its niche and prevent its resurgence. Species
with short generation times and high fecundity, such as
gelatinous animals and squids, are particularly suited to
the opportunistic replacement of vertebrates with late
maturity and fewer young (Lynam et al. 2006; Zeidberg
& Robison 2007). Replacement species may not feed on
the same mix of prey as those they succeed, producing a
differential effect on the deep community, its structure,
and its diversity.
Another way commercial fishing pressures may affect
deep pelagic biodiversity is by “fishing down the food
web” (Pauly et al. 1998). As the numbers of top predators have declined, fishing effort has shifted to species at
lower trophic levels. In some cases deep-living species
themselves, such as myctophid fishes (Valinassab et al.
2007) and Antarctic krill (Jones & Ramm 2004), have become targets for commercial fisheries. Commercial fishing for krill off the U.S. west coast has been banned in
state and federal waters to preclude the expansion of
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existing krill fisheries originating in Japan and Canada
(PFMC 2006).
High-Seas Fish Farming
The ecological impacts of present-day commercial aquaculture can be small or large, depending on how the facilities are operated. Recently, plans for large-scale, offshore
fish farms have been widely discussed (Naylor & Burke
2005; Naylor 2006), and these operations have the potential for significant ecological impact on deep pelagic
communities. Although the first steps for this development will be within national exclusive economic zones,
initial success may lead to operations in deep international waters.
No assessments have yet been made of how deep
pelagic communities might be affected, but the two obvious issues are input and output. If industrial-scale offshore fish farming incorporates natural productivity as its
food supply, then the normal food chain may be shortcircuited, reducing the natural food supply for the deep
pelagic community. If the captive populations are fed
with locally harvested wild stock (e.g., krill), then the surrounding natural populations may be depleted. Industrialscale organic discharge would also have an impact on the
deep community outside the enclosures. Requirements
for free-flowing water may lead to dispersal beyond the
enclosures of parasites and of compounds introduced to
enhance growth or reduce disease among the captive
fish. Likewise, organic wastes will infiltrate the surrounding waters. Expanding food production will continue to
be a major driving force behind the reduction of biodiversity and ecosystem services in the ocean as Earth’s
population continues to swell (Sarukhan 2006; Worm
et al. 2006).
Ballast Water
In addition to the redistribution of pathogens by ballast
water discharges, this vector is also a source of invasive colonization by the larvae of exotic pelagic species.
Invasion of the Black Sea by the ctenophore Mnemiopsis leidyi is well documented because that species lives
near the surface and is readily observed (Kideys 1994).
Expanding beyond the Black Sea, Mnemiopsis appears
to have few natural predators in the region, and it has
outcompeted the native ctenophores in some habitats.
Because this ctenophore’s food consists of zooplankton
and the eggs and larvae of fishes, regional anchovy fisheries important to Turkey and Russia were nearly wiped
out (Shiganova et al. 2001). If the natural transport of
planktonic larvae between regions by currents can be
likened to natural levels of genetic mutation, then ballast
water can be seen as a mutagen, accelerating the rate of
change.
Like Mnemiopsis, many deep-living species may be relocated because their larval stages live near the surface,
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but this prospect has yet to be considered in threat assessments. Member states adopted a new Ballast Water
Convention in 2004 (IMO 2005) that restricts discharges
within coastal regions. Nevertheless, the exchange of ballast water on the high seas is not only condoned but is
recommended. This practice is undoubtedly causing the
redistribution of deep-living species in offshore regions.
One alternative, the poisoning of ballast water with toxins, has obvious drawbacks. A promising, nontoxic approach calls for the deoxygenation of ballast water with
nitrogen to kill the larvae of potentially invasive species
(Tamburri et al. 2002).
Industrial Resuspension of Sediments
Most of the deep seafloor is covered with a thick layer
of sediment. This layer is easily resuspended, and once
disturbed it hangs in the water column for a very long
time. Industrial-scale activity on the deep seafloor will
inevitably create persistent clouds of resuspended sediments that reach hundreds of meters up into the water
column and spread laterally in currents (Jankowski &
Zielke 2001).
Among the most conspicuous inhabitants of the
pelagic fauna above the seafloor are filter-feeding larvaceans and carnivorous lobate ctenophores. Larvaceans
feed by building intricately structured, mucous filters
(Fig. 3g) that select small particles for ingestion, whereas
large particles build up externally. When the filters become too clogged for efficient water flow, the animal
discards them and builds new ones (Robison et al. 2005).
Thick, persistent clouds of resuspended sediment will
lead to an acceleration of the discard cycle, which is
delicately balanced with nutrient intake, and the extra
burden of accumulated particles on the outsides of the
filters will defeat the carefully maintained neutral buoyancy these animals must sustain. Likewise, ctenophores
will be beset with particle densities that will compromise the ciliary and mucosal motions that trap and help
them ingest their prey and will challenge their buoyancy
control. Mining of polymetallic sulfide deposits near hydrothermal vents will occur in areas with thinner sediment layers because the seafloor there is relatively new.
Nevertheless, perturbations in the form of toxic compounds and the pumping of ore from deep to shallow
water will occur (Halfar & Fujita 2007).
Expansion of Oxygen Minimum Layers
Oxygen minimum layers are depth zones in the water
column where the dissolved oxygen content is very low,
diminished by microbial oxidation of organic matter. Because of stratification, vertical mixing does not replenish
the oxygen. Many fewer animals and many fewer species
inhabit these layers than occur at depths above and below. Another consequence of climate change and increasing CO 2 input may be the expansion of oxygen minimum
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layers in many parts of the ocean and their creation in
places where they do not already exist (Keeling & Garcia 2002; Chan et al. 2008). The effects of such changes,
in general, will be to enhance ecological stratification
in the water column. Expanding the vertical extent of
existing layers will further separate many deep pelagic
species from their food sources in the upper layers and
may reduce the amount of food that sinks through. The
creation of new oxygen minimum layers in geographic
regions where they do not presently exist is equivalent
to desertification in terrestrial ecosystems.
Bioprospecting and Oil Extraction
At present, threat levels to deep pelagic animals from bioprospecting seem vanishingly small, although the potential for profitable discovery is high (Pomponi 2001). The
principal problems will arise after a promising biocompound is discovered. Ideally, laboratory synthesis should
provide adequate supplies for subsequent commercial
testing and development. Nevertheless, many marine
bioactive compounds are highly complex and difficult to
synthesize in the quantities necessary for industrial-scale
processing (Faulkner 2000). Thus, harvesting from the
natural habitat may be necessary. For screening purposes
the material requirements are small, but for development
stages, many tons may be necessary, bringing about the
threat. Selective harvesting of a deep pelagic species in
large quantities will be very challenging and will likely require indiscriminate, large-volume collecting. Problems
of bycatch and consequent damage to hundreds of other
species or to entire communities may ensue.
As offshore drilling technology evolves, rigs and platforms are moving ever deeper. In the Gulf of Mexico
drilling rigs are working in water depths over 2000 m,
and an exploratory well has been drilled in water 3000 m
deep. A consequence of offshore drilling is the discharge
of drilling fluids and cuttings. Drilling fluids are often recycled, but they are also released intermittently throughout
the drilling process. Their constituents include barite and
bentonite to increase density and viscosity. Toxicity studies, bioaccumulation studies, and field monitoring have
indicated relatively little negative impact from short-term
exposure to water-based drilling fluids (e.g., Neff et al.
1989), but only benthic animals have been studied. Nonaqueous drilling fluids have substantially higher negative
impact (Melton et al. 2000). Another type of discharge,
generated in high volumes from working offshore wells,
is “produced water” or water that has been trapped,
long-term, with oil and gas below the seafloor. Unlike
drilling fluids, which are associated only with drilling,
produced water is generated as long as the well is active.
Produced water may be treated to remove some contaminants before being discharged or recycled through the
well, depending on local regulations and compliance, but
polycyclic aromatic hydrocarbons remain as a particular
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concern for negative environmental impact, especially
for pelagic species (Durell et al. 2006). The effects of
these discharges on deep pelagic animals are unknown.
Iron Fertilization and Waste Disposal
The debate continues over whether it is useful or appropriate to artificially fertilize the ocean with iron to
draw down atmospheric levels of CO 2 (Chisholm et al.
2001; Buesseler & Boyd 2003). The effects of large-scale
fertilization on the deep pelagic fauna might include a
reduction in the oxygen content of the midwaters due
to the oxidation of sinking phytoplankton masses by microbes, and a restructuring of planktonic communities
near the surface due to species shifts among the targeted
phytoplankton (Koslow 2007). Either effect could have a
substantial impact on the deep-living biota.
In a progression of agreements from 1972 to 1996,
the London Convention and Protocol has led to international bans on the dumping of radioactive and other industrial wastes at sea (IMO 2003). Nevertheless, the deep
seabed has long been attractive as a site for depositing humankind’s worst waste products, based on the principle
of out of sight, out of mind. This alternative still has advocates. The principal problem with all such dumping is
that once these materials are on the deep seabed, they are
nearly impossible to extract if later it is determined to be
not such a good idea after all. For example, before it was
known how ephemeral polar ice sheets can be, they were
seriously considered as burial sites for long-term radioactive waste disposal (OTA 1985). The very remoteness and
inaccessibility of the deep ocean, factors that make it so
appealing as a dumping ground, are also what make it
so dangerous to consider. Once in place the transfer of
pollutants to the deep pelagic food web is most likely to
occur through contaminated sediments resuspended by
activity or currents and ingested by filter-feeding pelagic
animals, and through trophic transfer by benthopelagic
animals.
Policy Recommendations
Establish a Baseline
The oceans are in transition: rising temperatures, overfishing, acidification, and pollution are growing threats
that individually and interactively will have profound effects on deep oceanic biology. As the ocean’s stewards,
we must answer the following questions: How can the
effects of these changes be recognized, measured, and
evaluated? How can predictive capability be gained so
that policies can be developed that will positively affect
the deep oceans?
Biodiversity is a fundamental measure of ecosystems
that is widely used as a diagnostic indicator of environmental status. Sufficient data are lacking to determine
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the rates and directions of ongoing changes in the
biodiversity of deep pelagic systems or to identify and
quantify the ecosystem services they provide. With no
baseline, the problem cannot be assessed. To develop
such a baseline, the following fundamental questions
must be addressed: What practical definitions of biodiversity can be applied to this fauna? What are the ecologically
valid spatial scales that should be measured? What are the
appropriate temporal scales to investigate? What synoptic
environmental measurements must also be made? What
are the technological limitations and potential solutions?
The task of establishing a biodiversity baseline for the
deep pelagic biota is daunting if only because of the
sheer size of the habitat. Angel (1993) points out that
“[t]he scales of oceanic ecosystems are so large that the
methodologies developed for terrestrial conservation and
resource management are inapplicable.” Nevertheless,
this challenge can be met, and it is long past time we
started. As for locations, the large-scale patterns of pelagic
biodiversity are apparent from biogeographic investigations over the last century. Locality, exclusive of neritic
regions, is far less important than in terrestrial ecology
(Angel 1997), although local productivity levels affect diversity, biomass, and abundance and isolated populations
may be more common than expected (Miya & Nishida
1997).
The initial content of a baseline data set would be a list
of species and their relative abundances. Alternatives to
complete biodiversity baselines include the assessment
of functional ecological groupings at each trophic level,
such as guilds of predatory fishes or large, omnivorous
siphonophores. Another approach is to measure the diversity of taxonomic proxy groups (Solow 1995), such as
copepods or ctenophores.
Protected Areas
Efforts to conserve deep-sea biodiversity have focused
chiefly on seamounts, deep-sea corals, and damage by
indiscriminate bottom trawling (Watling & Norse 1998;
Thrush & Dayton 2002; Gianni 2004). Considerations of
pelagic protection have been directed at the conservation
of wide-ranging, epipelagic megafauna (Norse 2005b),
and because these animals are often migratory, the concept of a fixed area may be inappropriate. But for deep
pelagic animals, which are far less mobile, a geographically static protected area makes sense. The general concept of an open-ocean international reserve that included
the full water column and the deep seafloor was proposed
by Mills and Carlton (1998). They envisioned restrictions
on shipping, fishing, mining, dumping, weapons, and
floating cities. They also argued that such refuges should
be established soon, without holding out for more data
on the best location or optimal size.
Although this latter point might seem controversial,
the issue of moving quickly to begin protecting some
855
representative component of deep pelagic biodiversity
is not unreasonable. The question then becomes how
to select the areas to protect. The basic ocean-scale patterns of pelagic biogeography are well established (Angel
1997), and the identification of regions for conservation
that are typical of the major oceanic provinces would be
straightforward (Lourie & Vincent 2004). Likewise, the
spatial and temporal dynamics of basic ocean processes
that affect these provinces are well known. Biodiversity
hotspots (Myers et al. 2000) within the principal oceanic
provinces could define the location of suitable reserves.
Linking the protection of deep pelagic biodiversity to
deep benthic communities would be the most effective
approach to policy and management because the two
faunas are ecologically coupled.
Discussion
How is it that the greatest assemblage of animal species
on the planet has been largely overlooked in plans for
conserving marine biodiversity? The simple truth is that
they live in an immense and inaccessible habitat that is difficult to sample and even harder to visualize. The account
of threats presented here is incomplete, but it reflects the
scope of the challenges to deep pelagic biodiversity. Although some threats stem from resource extraction and
industrial use, climate change and acidification have an irreversible momentum that will build in the short term, regardless of human efforts at mitigation. These two forces
will directly and indirectly affect the deep pelagic biota
through the physiological effects of temperature change
and hypercapnia and through alterations in the food web
that supplies their nutrition. The underlying issue, regardless of the specific threat, is that this enormous reservoir
of animal diversity must be included when the implications of these developments are discussed.
Removing vertebrate top predators has had a profound
effect on biodiversity in coastal ecosystems. Historical reconstruction of ecosystems before their transformation
by human or natural influences is a valuable tool for conservation and restoration (Jackson 2001; Willis & Birks
2006), but in deep water the raw materials for attaining
historical perspectives may not be available. Although
we can apply lessons learned from coastal and terrestrial
ecosystems to the high seas, specific knowledge of what
was natural is elusive. In addition, there is the similar
problem of “shifting baseline syndrome” in fisheries science (Pauly 1995). Given the changes occurring in the
upper layers of the ocean, there can be little doubt that
substantive changes must be taking place in deeper waters as well. Yet because there is no baseline of species
composition and relative abundance for the deep pelagic
biota, we cannot quantify or evaluate those deep changes.
The longer we wait, the farther we will be from knowing
what constitutes a pristine natural system.
Conservation Biology
Volume 23, No. 4, 2009
856
Baseline studies could begin immediately because
there are no technological limitations or international
constraints, and the resource requirements for such an
effort are relatively small. The Census of Marine Life’s
MAR-ECO project reflects the broad scope of international expertise that can be successfully brought to bear
on this issue (Bergstad et al. 2008). Protected areas will
take more time to initiate and will require a greater effort,
if only for the requirements of international agreements.
But as Mills and Carlton (1988) argue, we should not wait
to get started.
The phrase protecting marine biodiversity on the
high seas is common language in most international
agreements regarding deep marine protected areas. But
the existing agreements focus almost exclusively on the
seabed (Ardron et al. 2008). An important policy development will be to change the substance of these agreements
to include protection of the full water column above the
seafloor as well. Recently, the scope of biodiversity protection language has begun to expand in international
agreements about protection of the high seas (e.g., IUCN
2008).
Another necessary policy initiative is to elevate the
level of public awareness about the existence of deep
pelagic animals and their significance in Earth’s biosphere. This immense resource is our common heritage,
and yet the high seas are still a frontier, and their exploitation takes place without regard for our common
good. Common sense tells us that the oceans should be
protected and that protection should include the conservation of deep pelagic biodiversity.
The single most important point of this review is the
salient fact that despite the global significance of the deep
pelagic fauna and the obvious benefits of protecting its
biodiversity, the basic information necessary to do so
is still lacking. There is no baseline. Even so, we must
begin the process of protecting deep pelagic biodiversity
without waiting for that job to be finished.
Acknowledgments
This work was supported by the David and Lucile Packard
Foundation, the Rockefeller Foundation through their
Bellagio Center, and N. Harray.
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